Key message
RLKs in anther development.
Abstract
The cell-to-cell communication is essential for specifying different cell types during plant growth, development and adaption to the ever-changing environment. Plant male reproduction, in particular, requires the exquisitely synchronized development of different cell layers within the male tissue, the anther. Receptor-like kinases (RLKs) belong to a large group of kinases localized on the cell surfaces, perceiving extracellular signals and thereafter regulating intracellular processes. Here we update the role of RLKs in early anther development by defining the cell fate and anther patterning, responding to the changing environment and controlling anther carbohydrate metabolism. We provide speculation of the poorly characterized ligands and substrates of these RLKs. The conserved and diversified aspects underlying the function of RLKs in anther development are discussed.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Albrecht C, Russinova E, Hecht V, Baaijens E, de Vries S (2005) The Arabidopsis thaliana SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASES1 and 2 control male sporogenesis. Plant Cell 17:3337–3349
Bethani I, Skanland SS, Dikic I, Acker-Palmer A (2010) Spatial organization of transmembrane receptor signalling. EMBO J 29:2677–2688. https://doi.org/10.1038/emboj.2010.175
Betsuyaku S, Takahashi F, Kinoshita A, Miwa H, Shinozaki K, Fukuda H, Sawa S (2011) Mitogen-activated protein kinase regulated by the CLAVATA receptors contributes to shoot apical meristem homeostasis. Plant Cell Physiol 52:14–29. https://doi.org/10.1093/pcp/pcq157
Brand U, Fletcher JC, Hobe M, Meyerowitz EM, Simon R (2000) Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. Science 289:617–619. https://doi.org/10.1126/science.289.5479.617
Canales C, Bhatt AM, Scott R, Dickinson H (2002) EXS, a putative LRR receptor kinase, regulates male germline cell number and tapetal identity and promotes seed development in Arabidopsis. Curr Biol 12:1718–1727. https://doi.org/10.1016/s0960-9822(02)01151-x
Cecchetti V, Altamura MM, Falasca G, Costantino P, Cardarelli M (2008) Auxin regulates Arabidopsis anther dehiscence, pollen maturation, and filament elongation. Plant Cell 20:1760–1774. https://doi.org/10.1105/tpc.107.057570
Chaturvedi P, Ischebeck T, Egelhofer V, Lichtscheidl I, Weckwerth W (2013) Cell-specific analysis of the tomato pollen proteome from pollen mother cell to mature pollen provides evidence for developmental priming. J Proteome Res 12:4892–4903. https://doi.org/10.1021/pr400197p
Chaubal R, Anderson JR, Trimnell MR, Fox TW, Albertsen MC, Bedinger P (2003) The transformation of anthers in the msca1 mutant of maize. Planta 216:778–788. https://doi.org/10.1007/s00425-002-0929-8
Chen R et al (2007) Rice UDP-glucose pyrophosphorylase1 is essential for pollen callose deposition and its cosuppression results in a new type of thermosensitive genic male sterility. Plant Cell 19:847–861. https://doi.org/10.1105/tpc.106.044123
Cock JM, McCormick S (2001) A large family of genes that share homology with CLAVATA3. Plant Physiol 126:939–942. https://doi.org/10.1104/pp.126.3.939
Colcombet J, Boisson-Dernier A, Ros-Palau R, Vera CE, Schroeder JI (2005) Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASES1 and 2 are essential for tapetum development and microspore maturation. Plant Cell 17:3350–3361
De Smet I, Voss U, Jurgens G, Beeckman T (2009) Receptor-like kinases shape the plant. Nat Cell Biol 11:1166–1173. https://doi.org/10.1038/ncb1009-1166
De Storme N, Geelen D (2014) The impact of environmental stress on male reproductive development in plants: biological processes and molecular mechanisms. Plant Cell Environ 37:1–18. https://doi.org/10.1111/pce.12142
DeYoung BJ, Bickle KL, Schrage KJ, Muskett P, Patel K, Clark SE (2006) The CLAVATA1-related BAM1, BAM2 and BAM3 receptor kinase-like proteins are required for meristem function in Arabidopsis. Plant J 45:1–16. https://doi.org/10.1111/j.1365-313X.2005.02592.x
Fei Q, Yang L, Liang W, Zhang D, Meyers BC (2016) Dynamic changes of small RNAs in rice spikelet development reveal specialized reproductive phasiRNA pathways. J Exp Bot 67:6037–6049. https://doi.org/10.1093/jxb/erw361
Feng X, Dickinson HG (2010) Tapetal cell fate, lineage and proliferation in the Arabidopsis anther. Development 137:2409–2416. https://doi.org/10.1242/dev.049320
Feng X, Zilberman D, Dickinson H (2013) A conversation across generations: soma-germ cell crosstalk in plants. Dev Cell 24:215–225. https://doi.org/10.1016/j.devcel.2013.01.014
Giorno F, Wolters-Arts M, Mariani C, Rieu I (2013) Ensuring reproduction at high temperatures: the heat stress response during anther and pollen development. Plants 2:489–506. https://doi.org/10.3390/plants2030489
Gomez JF, Talle B, Wilson ZA (2015) Anther and pollen development: a conserved developmental pathway. J Integr Plant Biol 57:876–891. https://doi.org/10.1111/jipb.12425
Guo J-X, Liu Y-G (2012) Molecular control of male reproductive development and pollen fertility in rice. J Integr Plant Biol 54:967–978. https://doi.org/10.1111/j.1744-7909.2012.01172.x
Hong L et al (2012a) MIL2 (MICROSPORELESS2) regulates early cell differentiation in the rice anther. New Phytol 196:402–413. https://doi.org/10.1111/j.1469-8137.2012.04270.x
Hong L, Tang D, Zhu K, Wang K, Li M, Cheng Z (2012b) Somatic and reproductive cell development in rice anther is regulated by a putative glutaredoxin. Plant Cell 24:577–588. https://doi.org/10.1105/tpc.111.093740
Hord CL, Chen CB, DeYoung BJ, Clark SE, Ma H (2006) The BAM1/BAM2 receptor-like kinases are important regulators of Arabidopsis early anther development. Plant Cell 18:1667–1680
Hord CL, Sun YJ, Pillitteri LJ, Torii KU, Wang H, Zhang S, Ma H (2008) Regulation of Arabidopsis early anther development by the mitogen-activated protein kinases, MPK3 and MPK6, and the ERECTA and related receptor-like kinases. Mol Plant 1:645–658. https://doi.org/10.1093/mp/ssn029
Hu L et al (2011) Rice MADS3 regulates ROS homeostasis during late anther development. Plant Cell 23:515
Huang J, Zhang T, Linstroth L, Tillman Z, Otegui MS, Owen HA, Zhao D (2016) Control of anther cell differentiation by the small protein ligand TPD1 and its receptor EMS1 in Arabidopsis. PLoS Genet 12:e1006147. https://doi.org/10.1371/journal.pgen.1006147
Huang J et al (2017) Carbonic anhydrases function in anther cell differentiation downstream of the receptor-like kinase EMS1. Plant Cell 29:1335–1356. https://doi.org/10.1105/tpc.16.00484
Hubbard SR, Till JH (2000) Protein tyrosine kinase structure and function. Annu Rev Biochem 69:373–398. https://doi.org/10.1146/annurev.biochem.69.1.373
Imin N, Kerim T, Weinman JJ, Rolfe BG (2001) Characterisation of rice anther proteins expressed at the young microspore stage. Proteomics 1:1149–1161. https://doi.org/10.1002/1615-9861(200109)1:9<1149::AID-PROT1149>3.0.CO;2-R
Indriolo E, Goring DR (2016) Yeast two-hybrid interactions between Arabidopsis lyrata S Receptor Kinase and the ARC1 E3 ligase. Plant Signal Behav 11:e1188233. https://doi.org/10.1080/15592324.2016.1188233
Ito T, Nagata N, Yoshiba Y, Ohme-Takagi M, Ma H, Shinozaki K (2007) Arabidopsis MALE STERILITY1 encodes a PHD-type transcription factor and regulates pollen and tapetum development. Plant Cell 19:3549
Jia G, Liu X, Owen HA, Zhao D (2008) Signaling of cell fate determination by the TPD1 small protein and EMS1 receptor kinase. Proc Natl Acad Sci USA 105:2220–2225. https://doi.org/10.1073/pnas.0708795105
Jun J et al (2010) Comprehensive analysis of CLE polypeptide signaling gene expression and overexpression activity in Arabidopsis. Plant Physiol 154:1721–1736. https://doi.org/10.1104/pp.110.163683
Kelliher T, Walbot V (2011) Emergence and patterning of the five cell types of the Zea mays anther locule. Dev Biol 350:32–49. https://doi.org/10.1016/j.ydbio.2010.11.005
Kelliher T, Walbot V (2012) Hypoxia triggers meiotic fate acquisition in maize. Science 337:345–348. https://doi.org/10.1126/science.1220080
Kerim T, Imin N, Weinman JJ, Rolfe BG (2003) Proteome analysis of male gametophyte development in rice anthers. Proteomics 3:738–751. https://doi.org/10.1002/pmic.200300424
Kim Y-J, Zhang D (2017) Molecular control of male fertility for crop hybrid breeding. Trends Plant Sci. https://doi.org/10.1016/j.tplants.2017.10.001
Kim M, Kim H, Lee W, Lee Y, Kwon S-W, Lee J (2015) Quantitative shotgun proteomics analysis of rice anther proteins after exposure to high temperature. Int J Genomics. 2015:9. https://doi.org/10.1155/2015/238704
Kinoshita A et al (2010) RPK2 is an essential receptor-like kinase that transmits the CLV3 signal in Arabidopsis. Development 137:3911–3920. https://doi.org/10.1242/dev.048199
Lee JS et al (2012) Direct interaction of ligand-receptor pairs specifying stomatal patterning. Genes Dev 26:126–136. https://doi.org/10.1101/gad.179895.111
Lemmon MA, Schlessinger J (2010) Cell signaling by receptor tyrosine kinases. Cell 141:1117–1134. https://doi.org/10.1016/j.cell.2010.06.011
Li S, Lauri A, Ziemann M, Busch A, Bhave M, Zachgo S (2009) Nuclear activity of ROXY1, a glutaredoxin interacting with tga factors, is required for petal development in Arabidopsis thaliana. Plant Cell 21:429
Li H, Shi Q, Zhang Z-B, Zeng L-P, Qi J, Ma H (2016) Evolution of the leucine-rich repeat receptor-like protein kinase gene family: ancestral copy number and functional divergence of BAM1 and BAM2 in Brassicaceae. J Syst Evol 54:204–218. https://doi.org/10.1111/jse.12206
Li ZY et al (2017) Two SERK receptor-like kinases interact with ems1 to control anther cell fate determination. Plant Physiol 173:326–337. https://doi.org/10.1104/pp.16.01219
Liao D, Cao Y, Sun X, Espinoza C, Nguyen CT, Liang Y, Stacey G (2017) Arabidopsis E3 ubiquitin ligase PLANT U-BOX13 (PUB13) regulates chitin receptor LYSIN MOTIF RECEPTOR KINASE5 (LYK5) protein abundance. New Phytol 214:1646–1656. https://doi.org/10.1111/nph.14472
Liu T et al (2012) Chitin-induced dimerization activates a plant immune receptor. Science 336:1160–1164. https://doi.org/10.1126/science.1218867
Ma H (2005) Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants. Annu Rev Plant Biol 56:393–434. https://doi.org/10.1146/annurev.arplant.55.031903.141717
Mariani C, Beuckeleer MD, Truettner J, Leemans J, Goldberg RB (1990) Induction of male sterility in plants by a chimaeric ribonuclease gene. Nature 347:737–741
Meng X et al (2015) Differential function of arabidopsis SERK family receptor-like kinases in stomatal patterning. Curr Biol 25:2361–2372. https://doi.org/10.1016/j.cub.2015.07.068
Millar AA, Gubler F (2005) The Arabidopsis GAMYB-like genes, MYB33 and MYB65, are microrna-regulated genes that redundantly facilitate anther development. Plant Cell 17:705
Mizuno S et al (2007) Receptor-like protein kinase2 (RPK2) is a novel factor controlling anther development in Arabidopsis thaliana. Plant J 50:751–766. https://doi.org/10.1111/j.1365-313X.2007.03083.x
Murmu J et al (2010) Arabidopsis basic leucine-zipper transcription factors TGA9 and TGA10 interact with floral glutaredoxins ROXY1 and ROXY2 and are redundantly required for anther development. Plant Physiol 154:1492–1504. https://doi.org/10.1104/pp.110.159111
Nam KH, Li J (2002) BRI1/BAK1, a receptor kinase pair mediating brassinosteroid signaling. Cell 110:203–212. https://doi.org/10.1016/S0092-8674(02)00814-0
Nguyen Q-N, Lee Y-S, Cho L-H, Jeong H-J, An G, Jung K-H (2015) Genome-wide identification and analysis of Catharanthus roseus RLK1-like kinases in rice. Planta 241:603–613. https://doi.org/10.1007/s00425-014-2203-2
Nonomura KI, Miyoshi K, Eiguchi M, Suzuki T, Miyao A, Hirochika H, Kurata N (2003) The MSP1 gene is necessary to restrict the number of cells entering into male and female sporogenesis and to initiate anther wall formation in rice. Plant Cell 15:1728–1739
Osakabe Y, Yamaguchi-Shinozaki K, Shinozaki K, Tran LSP (2013) Sensing the environment: key roles of membrane-localized kinases in plant perception and response to abiotic stress. J Exp Bot 64:445–458. https://doi.org/10.1093/jxb/ers354
Pillitteri LJ, Torii KU (2012) Mechanisms of stomatal development. Annu Rev Plant Biol 63:591–614. https://doi.org/10.1146/annurev-arplant-042811-105451
Pu CX et al (2017) The rice receptor-like kinases Dwarf And Runtish Spikelet1 And 2 repress cell death and affect sugar utilization during reproductive development. Plant Cell 29:70–89. https://doi.org/10.1105/tpc.16.00218
Qi Y, Sun Y, Xu L, Xu Y, Huang H (2004) ERECTA is required for protection against heat-stress in the AS1/AS2 pathway to regulate adaxial–abaxial leaf polarity in Arabidopsis. Planta 219:270–276. https://doi.org/10.1007/s00425-004-1248-z
Rieu I, Twell D, Firon N (2017) Pollen development at high temperature: from acclimation to collapse. Plant Physiol 173:1967–1976. https://doi.org/10.1104/pp.16.01644
Roberts MR, Boyes E, Scott RJ (1995) An investigation of the role of the anther tapetum during microspore development using genetic cell ablation. Sex Plant Reprod 8:299–307. https://doi.org/10.1007/bf00229387
Samuel MA, Mudgil Y, Salt JN, Delmas F, Ramachandran S, Chilelli A, Goring DR (2008) Interactions between the S-domain receptor kinases and AtPUB-ARM E3 ubiquitin ligases suggest a conserved signaling pathway in Arabidopsis. Plant Physiol 147:2084–2095. https://doi.org/10.1104/pp.108.123380
Schiefthaler U, Balasubramanian S, Sieber P, Chevalier D, Wisman E, Schneitz K (1999) Molecular analysis of NOZZLE, a gene involved in pattern formation and early sporogenesis during sex organ development in Arabidopsis thaliana. Proc Natl Acad Sci 96:11664–11669. https://doi.org/10.1073/pnas.96.20.11664
Shen H et al (2015) Overexpression of receptor-like kinase ERECTA improves thermotolerance in rice and tomato. Nat Biotechnol 33:996–1003. https://doi.org/10.1038/nbt.3321
Sheridan WF, Avalkina NA, Shamrov II, Batyea TB, Golubovskaya IN (1996) The MAC1 gene controlling the commitment to the meiotic pathway in maize. Genetics 142:1009
Sheridan WF, Golubeva EA, Abrhamova LI, Golubovskaya IN (1999) The mac1 mutation alters the developmental fate of the hypodermal cells and their cellular progeny in the maize anther. Genetics 153:933–941
Shimizu N et al (2015) BAM 1 and RECEPTOR-LIKE PROTEIN KINASE 2 constitute a signaling pathway and modulate CLE peptide-triggered growth inhibition in Arabidopsis root. New Phytol 208:1104–1113. https://doi.org/10.1111/nph.13520
Shiu SH, Bleecker AB (2001a) Plant receptor-like kinase gene family: diversity, function, and signaling. Sci STKE. 2001:re22 https://doi.org/10.1126/stke.2001.113.re22
Shiu SH, Bleecker AB (2001b) Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases. Proc Natl Acad Sci USA 98:10763–10768. https://doi.org/10.1073/pnas.181141598
Shiu SH, Karlowski WM, Pan R, Tzeng YH, Mayer KF, Li WH (2004) Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell 16:1220–1234. https://doi.org/10.1105/tpc.020834
Shpak ED, McAbee JM, Pillitteri LJ, Torii KU (2005) Stomatal patterning and differentiation by synergistic interactions of receptor kinases. Science 309:290–293. https://doi.org/10.1126/science.1109710
Smyth DR, Bowman JL, Meyerowitz EM (1990) Early flower development in Arabidopsis. Plant Cell. 2:755
Song W, Han ZF, Wang JZ, Lin GZ, Chai JJ (2017) Structural insights into ligand recognition and activation of plant receptor kinases. Curr Opin Plant Biol 43:18–27. https://doi.org/10.1016/j.sbi.2016.09.012
Sorensen A, Guerineau F, Canales-Holzeis C, Dickinson HG, Scott RJ (2002) A novel extinction screen in Arabidopsis thaliana identifies mutant plants defective in early microsporangial development. Plant J 29:581–594. https://doi.org/10.1046/j.0960-7412.2001.01240.x
Stegmann M et al (2017) The receptor kinase FER is a RALF-regulated scaffold controlling plant immune signaling. Science 355:287–289. https://doi.org/10.1126/science.aal2541
Stone JM, Walker JC (1995) Plant protein kinase families and signal transduction. Plant Physiol 108:451
Sun Y-J, Hord CLH, Chen C-B, Ma H (2007) regulation of Arabidopsis early anther development by putative cell-cell signaling molecules and transcriptional regulators. J Integr Plant Biol 49:60–68. https://doi.org/10.1111/j.1744-7909.2006.00408.x
Thorstensen T, Grini PE, Mercy IS, Alm V, Erdal S, Aasland R, Aalen RB (2008) The Arabidopsis SET-domain protein ASHR3 is involved in stamen development and interacts with the bHLH transcription factor ABORTED MICROSPORES (AMS). Plant Mol Biol 66:47–59. https://doi.org/10.1007/s11103-007-9251-y
Tian HQ, Kuang A, Musgrave ME, Russell SD (1998) Calcium distribution in fertile and sterile anthers of a photoperiod-sensitive genic male-sterile rice. Planta 204:183–192. https://doi.org/10.1007/s004250050245
Ullrich A, Schlessinger J (1990) Signal transduction by receptors with tyrosine kinase activity. Cell 61:203–212. https://doi.org/10.1016/0092-8674(90)90801-k
Uváčková Ľ, Takáč T, Boehm N, Obert B, Šamaj J (2012) Proteomic and biochemical analysis of maize anthers after cold pretreatment and induction of androgenesis reveals an important role of anti-oxidative enzymes. J Proteomics 75:1886–1894. https://doi.org/10.1016/j.jprot.2011.12.033
Walbot V, Egger RL (2016) Pre-meiotic anther development: cell fate specification and differentiation. Annu Rev Plant Biol 67:365–395. https://doi.org/10.1146/annurev-arplant-043015-111804
Walker JC (1994) Structure and function of the receptor-like protein kinases of higher plants. Plant Mol Biol 26:1599–1609. https://doi.org/10.1007/BF00016492
Wan J, Patel A, Mathieu M, Kim SY, Xu D, Stacey G (2008) A lectin receptor-like kinase is required for pollen development in Arabidopsis. Plant Mol Biol 67:469–482. https://doi.org/10.1007/s11103-008-9332-6
Wang H, Ngwenyama N, Liu Y, Walker JC, Zhang S (2007) Stomatal development and patterning are regulated by environmentally responsive mitogen-activated protein kinases in Arabidopsis. Plant Cell 19:63–73. https://doi.org/10.1105/tpc.106.048298
Wang H, Lu Y, Jiang T, Berg H, Li C, Xia Y (2013) The Arabidopsis U–box/ARM repeat E3 ligase AtPUB4 influences growth and degeneration of tapetal cells, and its mutation leads to conditional male sterility. Plant J 74:511–523. https://doi.org/10.1111/tpj.12146
Wang Y et al (2014) Assessment of BAK1 activity in different plant receptor-like kinase complexes by quantitative profiling of phosphorylation patterns. J Proteomics 108:484–493. https://doi.org/10.1016/j.jprot.2014.06.009
Wang J et al (2015) The E3 ligase OsPUB15 interacts with the receptor-like kinase PID2 and regulates plant cell death and innate immunity. BMC Plant Biol 15:49. https://doi.org/10.1186/s12870-015-0442-4
Wilson ZA, Zhang D-B (2009) From Arabidopsis to rice: pathways in pollen development. J Exp Bot 60:1479–1492. https://doi.org/10.1093/jxb/erp095
Yang WC, Ye D, Xu J, Sundaresan V (1999) The SPOROCYTELESS gene of Arabidopsis is required for initiation of sporogenesis and encodes a novel nuclear protein. Gene Dev 13:2108–2117
Yang S-L et al (2003) TAPETUM DETERMINANT1 is required for cell specialization in the Arabidopsis anther. Plant Cell 15:2792–2804. https://doi.org/10.1105/tpc.016618
Yang L, Qian XL, Chen MJ, Fei QL, Meyers BC, Liang WQ, Zhang DB (2016) Regulatory role of a receptor-like kinase in specifying anther cell identity. Plant Physiol 171:2085–2100. https://doi.org/10.1104/pp.16.00016
Ye Q, Zhu W, Li L, Zhang S, Yin Y, Ma H, Wang X (2010) Brassinosteroids control male fertility by regulating the expression of key genes involved in Arabidopsis anther and pollen development. Proc Natl Acad Sci USA 107:6100–6105. https://doi.org/10.1073/pnas.0912333107
Ye J et al (2015) Proteomic and phosphoproteomic analyses reveal extensive phosphorylation of regulatory proteins in developing rice anthers. Plant J 84:527–544. https://doi.org/10.1111/tpj.13019
Ye J, Zhang Z, You C, Zhang X, Lu J, Ma H (2016) Abundant protein phosphorylation potentially regulates Arabidopsis anther development. J Exp Bot 67:4993–5008. https://doi.org/10.1093/jxb/erw293
Yu F, Tian W, Luan S (2014) From receptor-like kinases to calcium spikes: what are the missing links? Mol Plant 7:1501–1504. https://doi.org/10.1093/mp/ssu092
Yu J et al (2016) A rice ca2+ binding protein is required for tapetum function and pollen formation. Plant Physiol 172:1772–1786. https://doi.org/10.1104/pp.16.01261
Yu J et al (2017) Two rice receptor-like kinases maintain male fertility under changing temperatures. Proc Natl Acad Sci USA 114:12327–12332. https://doi.org/10.1073/pnas.1705189114
Zhang S, Klessig DF (2001) MAPK cascades in plant defense signaling. Trends Plant Sci 6:520–527. https://doi.org/10.1016/s1360-1385(01)02103-3
Zhang D, Yang L (2014) Specification of tapetum and microsporocyte cells within the anther. Curr Opin Plant Biol 17:49–55. https://doi.org/10.1016/j.pbi.2013.11.001
Zhang W, Sun Y, Timofejeva L, Chen C, Grossniklaus U, Ma H (2006) Regulation of Arabidopsis tapetum development and function by DYSFUNCTIONAL TAPETUM1 (DYT1) encoding a putative bHLH transcription factor. Development 133:3085–3095. https://doi.org/10.1242/dev.02463
Zhang H, Liang W, Yang X, Luo X, Jiang N, Ma H, Zhang D (2010) Carbon Starved Anther encodes a myb domain protein that regulates sugar partitioning required for rice pollen development. Plant Cell 22:672
Zhang D, Luo X, Zhu L (2011a) Cytological analysis and genetic control of rice anther development. J Genet Genomics 38:379–390. https://doi.org/10.1016/j.jgg.2011.08.001
Zhang H, Cao Y, Zhao J, Li X, Xiao J, Wang S (2011b) A pair of orthologs of a leucine-rich repeat receptor kinase-like disease resistance gene family regulates rice response to raised temperature. BMC Plant Biol 11:160. https://doi.org/10.1186/1471-2229-11-160
Zhang H et al (2013) Mutation in CSA creates a new photoperiod-sensitive genic male sterile line applicable for hybrid rice seed production. Proc Natl Acad Sci USA 110:76–81. https://doi.org/10.1073/pnas.1213041110
Zhao D (2009) Control of anther cell differentiation: a teamwork of receptor-like kinases. Sex Plant Reprod 22:221–228. https://doi.org/10.1007/s00497-009-0106-3
Zhao D-Z, Wang G-F, Speal B, Ma H (2002) The EXCESS MICROSPOROCYTES1 gene encodes a putative leucine-rich repeat receptor protein kinase that controls somatic and reproductive cell fates in the Arabidopsis anther. Genes Dev 16:2021–2031. https://doi.org/10.1101/gad.997902
Zhao X et al (2008) OsTDL1A binds to the LRR domain of rice receptor kinase MSP1, and is required to limit sporocyte numbers. Plant J 54:375–387. https://doi.org/10.1111/j.1365-313X.2008.03426.x
Zhao F et al (2017) Phosphorylation of SPOROCYTELESS/NOZZLE by the MPK3/6 kinase is required for anther development. Plant Physiol 173:2265–2277. https://doi.org/10.1104/pp.16.01765
Zhu J et al (2008) Defective in Tapetal development and function 1 is essential for anther development and tapetal function for microspore maturation in Arabidopsis. Plant J 55:266–277. https://doi.org/10.1111/j.1365-313X.2008.03500.x
Acknowledgements
This research was supported by the National Natural Science Foundation of China (Grants 31430009, 31322040, and 31271698); the National Key Research and Development Program of China (Grants 2016YFD0100804 and 2016YFE0101000); National Key Basic Research Development Program of the Ministry of Science and Technology, China (Grant 2013 CB126902); the Innovative Research Team, Ministry of Education, and 111 Project (Grant B14016); the Science and Technology Commission of Shanghai Municipality (Grant 13JC1408200); Australia-China Science and Research Fund Joint Research Centre (Grant ACSRF48187); the National Transgenic Major Program (Grant 2016ZX08009003-003-007); and W. Cai is supported by China Postdoctoral Science Foundation (Grant 2017M621451).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Additional information
A contribution to the special issue ‘Plant Reproduction Research in Asia’.
Rights and permissions
About this article
Cite this article
Cai, W., Zhang, D. The role of receptor-like kinases in regulating plant male reproduction. Plant Reprod 31, 77–87 (2018). https://doi.org/10.1007/s00497-018-0332-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00497-018-0332-7